Abstract
Electrical signals, including action potential (AP), play an important role in plant adaptation to the changing environmental conditions. Experimental and theoretical investigations of the mechanisms of AP generation are required to understand the relationships between environmental factors and electrical activity of plants. In this work we have elaborated a mathematical model of AP generation, which takes into account the participation of vacuole in the generation of electrical response. The model describes the transporters of the plasma membrane (Ca2+, Cl–, and K+ channels, H+- and Ca2+-ATPases, H+/K+ antiporter, and 2H+/Cl– symporter) and the tonoplast (Ca2+, Cl–, and K+ channels; H+- and Ca2+-ATPases; H+/K+, 2H+/Cl–, and 3H+/Ca2+ antiporters), with due consideration of their regulation by second messengers (Ca2+ and IP3). The apoplastic, cytoplasmic and vacuolar buffers are also described. The properties of the simulated AP are in good agreement with experimental data. The AP model describes the attenuation of electrical signal with an increase in the vacuole area and volume; this effect is related to a decrease in the Ca2+ spike magnitude. The electrical signal was weakly influenced by the K+ and Cl– content in the vacuole. It was also shown that the contribution of vacuolar IP3-dependent Ca2+ channels into the generation of calcium spike during AP was insignificant with the given parameters of the model. The results provide theoretical evidence for the significance of the vacuolar area and volume in plant cell excitability.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Martonosi A.N. 2000. Animal electricity, Ca2+ and muscle contraction. A brief history of muscle research. Acta Biochim. Pol. 47, 493–516.
Burdon-Sanderson J. 1873. Note on the electrical phenomena which accompany stimulation of the leaf of Dionaea muscipula. Philos. Proc. R. Soc. Lond. 21, 495–496.
Bose J.C. 1926. The nervous mechanism of plant. London: Longmans, Green et Co.
Trebacz K., Zawadzki T. 1985. Light-triggered action potentials in the liverwort Conocephalum conicum. Physiol. Plant. 64, 482–486.
Opritov V.A., Pyatygin S.S., Retivin V.G. 1991. Bioelektrogenez u vysshikh rasteniy (Bioelectrogenesis in Higher Plants), Moscow: Nauka.
Stahlberg R., Cleland R.E., Volkenburgh E. 2006. Slow wave potentials–a propagating electrical signal unique to higher plants. In: Communication in Plants. Baluška F., Mancuso S., Volkmann D., Eds. Berlin Heidelberg: Springer-Verlag, pp. 291–308.
Fromm J., Spanswick R. 1993. Characteristics of action potentials in willow (Salix viminalis L.). J. Exp. Bot. 44, 1119–1125.
Felle H.H., Zimmermann M.R. 2007. Systemic signalling in barley through action potentials. Planta. 226, 203–214.
Król E., Dziubinska H., Trebacz K. 2010. What do plants need action potentials for? In: Action potential: Biophysical and cellular context, initiation, phases and propagation. DuBois M.L., Ed. New York: Nova Sci. Publ., pp. 1–26.
Shiina T., Tazawa M. 1986. Action potential in Luffa cylindrical and its effects on elongation growth. Plant Cell. Physiol. 27, 1081–1089.
Trebacz K., Dziubinska H., Król E. 2006. Electrical signals in longdistance communication in plants. In: Communication in plants. Neuronal aspects of plant life. Baluska F., Mancuso S., Volkmann D., Eds. Berlin: Springer, pp. 277–290.
Retivin V.G., Opritov V.A., Abramova N.N., Lobov S.A., Fedulina S.B. 1999. The ATP level in phloem exudates from the stem of a higher plant after the propagation of electrical responses to burn and cooling. Vestn. Nizhegorodskogo universiteta im. N.I. Lobachevskogo. Biology series. (Rus.). 1, 124–131.
Surova L., Sherstneva O., Vodeneev V., Katicheva L., Semina M., Sukhov V. 2016. Variation potentialinduced photosynthetic and respiratory changes increase ATP content in pea leaves. J. Plant Physiol. 202, 57–64. doi 10.1016/j.jplph.2016.05.024
Fromm J., Lautner S. 2007. Electrical signals and their physiological significance in plants. Plant Cell Environ. 30, 249–257.
Sinyukhin A.M. 1973. Functional activity of action potential in ferns and mosses during fertilization. Biofizika (Rus.). 18, 477–482.
Sukhov V. 2016. Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth. Res. 130, 373–387. doi 10.1007/s11120-016-0270-x
Koziolek C., Grams T.E.E., Schreiber U., Matyssek R., Fromm J. 2004. Transient knockout of photosynthesis mediated by electrical signals. New Phytol. 161, 715–722.
Lautner S., Grams T.E.E., Matyssek R., Fromm J. 2005. Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol. 138, 2200–2209.
Pavlovic A., Slováková L., Pandolfi C., Mancuso S. 2011. On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). J. Exp. Bot. 62, 1991–2000.
Dziubinska H., Trebacz K., Zawadzki T. 1989. The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum. Physiol. Plant. 75, 417–423.
Retivin V.G., Opritov V.G., Fedulina S.B. 1997. Action potential-induced preadaptation of tissues of the Cucurbita pepo stem to the damaging effect of low temperatures. Fiziologiya rasteniy (Rus.). 44, 499–510.
Opritov V.A. 1998. Funktsional’nye aspekty bioelektrogeneza u vysshikh rasteniy. 59-e Timiryazevskoye chteniye (Functional aspects of bioelectrogenesis in higher plants. The 59th Timiryazev readings). Nizhny Novgorod: NNGU.
Sukhov V., Surova L., Sherstneva O., Bushueva A., Vodeneev V. 2015. Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. Funct. Plant Biol. 42, 727–736.
Surova L., Sherstneva O., Vodeneev V., Sukhov V. 2016. Variation potential propagation decreases heatrelated damage of pea photosystem I by 2 different pathways. Plant Sign. Behav. 11, e1145334.
Vodeneev V.A., Opritov V.A., Pyatygin S.S. 2006. Reversible change in intracellular pH during action potential generation in the higher plant Cucurbita pepo. Russ. J. Plant Physiol. 53, 538–545.
Swarbreck S.M., Colaço R., Davies J.M. 2013. Plant calcium-permeable channels. Plant Physiol. 163, 514–522.
Jammes F., Hu H.-C., Villiers F., Bouten R., Kwak J.M. 2011. Calcium-permeable channels in plant cells. FEBS J. 278, 4262–4276.
Plieth C. 1999. Temperature sensing by plants: Calcium-permeable channels as primary sensors–a model. J. Membr. Biol. 172, 121–127.
Carpaneto A., Ivashikina N., Levchenko V., Krol E., Jeworutzki E., Zhu J.-K., Hedrich R. 2007. Cold transiently activates calcium-permeable channels in Arabidopsis mesophyll cells. Plant Physiol. 143, 487–494.
Trebacz K., Tarnecki R., Zawadzki T. 1989. The effect of ionic channel inhibitors and factors modifying metabolism on the excitability of the liverwort Conocephalum conicum. Physiol. Plant. 75, 24–30.
Krol E., Dziubinska H., Trebacz K. 2004. Low-temperature-induced transmembrane potential changes in mesophyll cells of Arabidopsis thaliana, Helianthus annuus and Vicia faba. Physiol. Plant. 120, 265–270.
Lewis B.D., Karlin-Neumann G., Davis R.W., Spalding E.P. 1997. Ca{u2+}-activated anion channels and membrane depolarizations induced by blue light and cold in Arabidopsis seedlings. Plant Physiol. 114, 1327–1334.
Opritov V.A., Pyatygin S.S., Vodeneev V.A. 2002. Direct coupling of generation in the cells of the higher plant Cucurbita pepo L. with the work of electrogenic pump. Russ. J. Plant Physiol. 49, 534–542.
Shimmen T., Mimura T., Kikuyama M., Tazawa M. 1994. Characean cells as a tool for studying electrophysiological characteristics of plant cell structure and function. Cell Struct. Funct. 19, 263–278.
Beilby M.J. 2007. Action potential in charophytes. Int. Rev. Cytol. 257, 43–82.
Kikuyama M., Tazawa M. 1976. Tonoplast action potential in Nitella in relation to vacuolar chloride concentration. J. Membr. Biol. 29, 95–110.
Hedrich R. 2012. Ion channels in plants. Physiol. Rev. 92, 1777–1811.
Isayenkov S., Isner J.C., Maathuis F.J.M. 2010. Vacuolar ion channels: Roles in plant nutrition and signaling. FEBS Lett. 584, 1982–1988.
Reisen D., Marty F., Leborgne-Castel N. 2005. New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol. 5, 13.
Marty F. 1999. Plant vacuoles. Plant Cell. 11, 587–599.
Stael S., Wurzinger B., Mair A., Mehlmer N., Vothknecht U.C., Teige M. 2012. Plant organellar calcium signalling: An emerging field. J. Exp. Bot. 63, 1525–1542.
Barkla B.J., Pantoja O. 1996. Physiology of ion transport across the tonoplast of higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 159–184.
Biskup B., Gradmann D., Thiel G. 1999. Calcium release from InsP3-sensitive internal stores initiates action potential in Chara. FEBS Lett. 453, 72–76.
Wacke M., Thiel G., Hütt M.-T. 2003. Ca{u2+} dynamics during membrane excitation of green alga Chara: Model simulations and experimental data. J. Membr. Biol. 191, 179–192.
Beilby M.J. 1982. C1–channels in Chara. R. Soc._London B. 299, 435–445.
Mummert H., Gradmann D. 1991. Action potentials in Acetabularia: Measurement and simulation of voltagegated fluxes. J. Membr. Biol. 124, 265–273.
Gradmann D., Blatt M.R., Thiel G. 1993. Electrocoupling of ion transporters in plants. J. Membr. Biol. 136, 327–332.
Gradmann D., Johannes E., Hansen U.-P. 1997. Kinetic anaylsis of Ca{u2+}/K+ selectivity of an ion channel by single-binding-site models. J. Membr. Biol. 159, 169–178.
Gradmann D. 2001. Impact of apoplast volume on ionic relations in plant cells. J. Membr. Biol. 184, 61–69.
Sukhov V., Vodeneev V. 2009. Mathematical model of action potential in cells of vascular plants. J. Membr. Biol. 232, 59–67.
Sukhov V., Nerush V., Orlova L., Vodeneev V. 2011. Simulation of action potential propagation in plants. J. Theor. Biol. 291, 47–55.
Hodgkin A.L., Huxley A.F. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544.
Schroeder J.I., Fang H.H. 1991. Inward-rectifying K+ channels in guard cells provide a mechanism for lowaffinity K+ uptake. Proc. Natl. Acad. Sci. USA. 88, 11583–11587.
Piñeros M., Tester M. 1996. Calcium channels in higher plant cells: Selectivity, regulation and pharmacology. J. Exp. Bot. 48, 551–577.
White P.J., Davenport R.J. 2002. The voltage-independent cation channel in the plasma membrane of wheat roots is permeable to divalent cations and may be involved in cytosolic Ca{u2+} homeostasis. Plant Physiol. 130, 1386–1395.
Halm D.R., Frizzell R.A. 1992. Anion permeation in an apical membrane chloride channel of a secretory epithelial cell. J. Gen. Physiol. 99, 339–366.
Nayyar H. 2003. Calcium as environmental sensor in plants. Curr. Sci. 84, 893–902.
Wacke M., Thiel G. 2001. Electrically triggered all-ornone Ca{u2+}-liberation during action potential in the giant alga Chara. J. Gen. Physiol. 118, 11–21.
DeWald D.B., Torabinejad J., Jones C.A, Shope J.C., Cangelosi A.R, Thompson J.E., Prestwich G.D., Hama H. 2001. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in saltstressed Arabidopsis. Plant Physiol. 126, 759–769.
Hansen U.-P., Gradmann D., Sanders D., Slayman C.L. 1981. Interpretation of current–voltage relationships for “active” ion transport systems: I. Steady-state reaction-kinetic analysis of class-I mechanisms. J. Membr. Biol. 63, 165–190.
Gradmann D., Boyd C.M. 2005. Apparent charge of binding site in ion-translocating enzymes: Kinetic impact. Eur. Biophys. J. 34, 353–357.
Pfanz H., Heber U. 1986. Buffer capacities of leaves, leaf cells, and leaf cell organelles in relation to fluxes of potentially acidic gases. Plant Physiol. 81, 597–602.
Tuteja N. 2009. Integrated calcium signaling in plants. In: Signaling in Plants. Baluska F., Mancuso S., Eds. Berlin–Heidelberg: Springer-Verlag, pp. 29–40.
Liu J., Whalley H.J., Knight M.R. 2015. Combining modelling and experimental approaches to explain how calcium signatures are decoded by calmodulin-binding transcription activators (CAMTAs) to produce specific gene expression responses. New Phytol. 208, 1–14.
Barbier-Brygoo H., Vinauger M., Colcombet J., Ephritikhine G., Frachisse J.-M., Maurel C. 2000. Anion channels in higher plants: Functional characterization, molecular structure and physiological role. Biochim. Biophys. Acta. 1465, 199–218.
Randall S.K. 1992. Characterization of vacuolar calcium-binding proteins. Plant Physiol. 100, 859–867.
Greenwald I. 1938. The dissociation of some calcium salts. J. Biol. Chem. 124, 437–452.
Colcombet J., Thomine S., Guern J., Frachisse J.-M., Barbier-Brygoo H. 2001. Nucleotides provide a voltage-sensitive gate for the rapid anion channel of Arabidopsis hypocotyl cells. J. Biol. Chem. 276, 36139–36145.
Zhang W.-H., Walker N.A., Patrick J.W., Tyerman S.D. 2004. Pulsing Cl–channels in coat cells of developing bean seeds linked to hypo-osmotic turgor regulation. J. Exp. Bot. 55, 993–1001.
Berestovsky G.N., Kataev A.A. 2005. Voltage-gated calcium and Ca{u2+}-activated chloride channels and Ca2+ transients: Voltage-clamp studies of perfused and intact cells of Chara. Eur. Biophys. J. 34, 973–986.
Brüggemann L., Dietrich P., Becker D., Dreyer I., Palme K., Hedrich R. 1999. Channel-mediated highaffinity K+ uptake into guard cells from Arabidopsis. Proc. Natl. Acad. Sci. USA. 96, 3298–3302.
Hills A., Chen Z.-H., Amtmann A., Blatt M.R., Lew V.L. 2012. OnGuard, a Computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiol. 159, 1026–1042.
Kinoshita T., Nishimura M., Shimazakib K. 1995. Cytosolic concentration of Ca{u2+} regulates the plasma membrane H+-ATPase in guard cells of Fava bean. Plant Cell. 7, 1333–1342.
Tikhonova L.I., Pottosin I.I., Dietz K.-J., Schbnknecht G. 1997. Fast-activating cation channel in barley mesophyll vacuoles. Inhibition by calcium. Plant J. 11, 1059–1070.
Gobert A., Isayenkov S., Voelker C., Czempinski K., Maathuis F.J. M. 2007. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc. Natl. Acad. Sci. USA. 104, 10726–10731.
Alexandre J., Lassalles J.P., Kado R.T. 1990. Opening of Ca{u2+} channels in isolated red beet root vacuole membrane by inositol 1,4,5-trisphosphate. Nature. 343, 567–570.
Plant P.J., Gelli A., Blumwald E. 1994. Vacuolar chloride regulation of an anion-selective tonoplast channel. J. Membr. Biol. 140, 1–12.
Hafke J.B., Hafke Y., Smith J.A.C., Lüttge U., Thiel G. 2003. Vacuolar malate uptake is mediated by an anionselective inward rectifier. Plant J. 35, 116–128.
Gambale F., Kolb H.A., Cant A.M., Hedrieh R. 1994. The voltage-dependent H+-ATPase of the sugar beet vacuole is reversible. Eur. Biophys. J. 22, 399–403.
Davies J. M., Hunt I., Sanders D. 1994. Vacuolar H+-pumping ATPase variable transport coupling ratio controlled by pH. Plant Biol. 91, 8547–8551.
Askerlund P., Evans D.E. 1992. Reconstitution and characterization of a calmodulin-stimulated Ca{u2+}-pumping ATPase purified from Brassica oleracea L. Plant Physiol. 100, 1670–1681.
Martinoia E., Maeshima M., Neuhaus H.E. 2007. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58, 83–102.
Etxeberria E., Pozueta-Romero J., Gonzalez P. 2012. In and out of the plant storage vacuole. Plant Sci. 190, 52–61.
Davies J.M. 1996. Vacuolar energization: Pumps, shunts and stress. J. Exp. Bot. 48, 633–641.
Sherstneva O.N., Vodeneev V.A., Katicheva L.A., Surova L.M., Sukhov V.S. 2015. Involvement of the changes in intra-and extracellular pH in the development of variable potential-induced photosynthetic response in pumpkin sprouts. Biochemistry (Mosc.). 80, 776–784.
Pyatygin S.S., Opritov V.A., Khudyakov V.A. 1992. Subthreshold changes in excitable membranes of Cucurbita pepo L. stem cells during cooling-induced action-potential generation. Planta. 186, 161–165.
Opritov V.A., Lobov S.A., Pyatygin S.S., Mysyagin S.A. 2005. Analysis of possible involvement of local bioelectric responses in chilling perception by higher plants exemplified by Cucurbita pepo. Russ. J. Plant Physiol. 52 (6), 801–808.
Krol E., Dziubinska H., Stolarz M., Trebacz K. 2006. Effects of ion channel inhibitors on cold and electrically induced action potentials in Dionaea muscipula. Biol. Plant. 50, 411–416.
Pyatygin S.S., Opritov V.A., Polovinkin A.V., Vodeneev V.A. 1999. On the nature of action potential of the higher plants. Dokl. Akademii nauk (Rus.). 366, 404–407.
Vodeneev V.A., Sherstneva O.N., Surova L.M., Semina M.M., Katicheva L.A., Sukhov V.S. 2016. Agedependent changes of photosynthetic responses induced by electrical signals in wheat seedlings. Russ. J. Plant Physiol. 63 (6), 861–868.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © E.M. Novikova, V.A. Vodeneev, V.S. Sukhov, 2017, published in Biologicheskie Membrany, 2017, Vol. 34, No. 2, pp. 109–125.
Rights and permissions
About this article
Cite this article
Novikova, E.M., Vodeneev, V.A. & Sukhov, V.S. Mathematical model of action potential in higher plants with account for the involvement of vacuole in the electrical signal generation. Biochem. Moscow Suppl. Ser. A 11, 151–167 (2017). https://doi.org/10.1134/S1990747817010068
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1990747817010068